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European Child & Adolescent Psychiatry

, Volume 26, Issue 8, pp 957–967 | Cite as

Further evidence for the role of pregnancy-induced hypertension and other early life influences in the development of ADHD: results from the IDEFICS study

  • Hermann PohlabelnEmail author
  • Stefan Rach
  • Stefaan De Henauw
  • Gabriele Eiben
  • Wencke Gwozdz
  • Charalampos Hadjigeorgiou
  • Dénes Molnár
  • Luis A. Moreno
  • Paola Russo
  • Toomas Veidebaum
  • Iris Pigeot
  • On behalf of the IDEFICS consortium
Original Contribution

Abstract

The aim of this study is to investigate whether in addition to established early risk factors other, less studied pre-, peri-, and postnatal influences, like gestational hypertension or neonatal respiratory disorders and infections, may increase a child’s risk of developing attention-deficit/hyperactivity disorders (ADHD). In the IDEFICS study more than 18,000 children, aged 2–11.9 years, underwent extensive medical examinations supplemented by parental questionnaires on pregnancy and early childhood. The present analyses are restricted to children whose parents also completed a supplementary medical questionnaire (n = 15,577), including the question whether or not the child was ever diagnosed with ADHD. Multilevel multivariable logistic regression was used to assess the association between early life influences and the risk of ADHD. Our study confirms the well-known association between maternal smoking during pregnancy and a child’s risk of ADHD. In addition, our study showed that children born to mothers younger than 20 years old were 3–4 times more likely to develop ADHD as compared to children born to mothers aged 25 years and older. Moreover, we found that children whose mothers suffered from pregnancy-induced hypertension had an approximately twofold risk of ADHD (OR 1.95; 95% CI 1.09–3.48). This also holds true for infections during the first 4 weeks after birth (OR 2.06; 95% CI 1.05–4.04). In addition, although not statistically significant, we observed a noticeable elevated risk estimate for neonatal respiratory disorders (OR 1.76; 95% CI 0.91–3.41). Hence, we recommend that these less often studied pre-, peri, and postnatal influences should get more attention when considering early indicators or predictors for ADHD in children. However, special study designs such as genetically sensitive designs may be needed to derive causal conclusions.

Keywords

Attention-deficit/hyperactivity disorders European children cohort Gestational hypertension Maternal age Neonatal respiratory disorders Smoking 

Notes

Acknowledgements

This work was done as part of the IDEFICS study (http://www.idefics.eu). We gratefully acknowledge the financial support of the European Community within the Sixth RTD Framework Programme Contract No. 016181 (FOOD) and the grant support from EU for IDEFICS study. We thank the children and their parents for their participation in the IDEFICS study. Finally, we would also like to thank the anonymous reviewers for their helpful comments and suggestions, which we have addressed in the revised manuscript.

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

References

  1. 1.
    Harpin VA (2005) The effect of ADHD on the life of an individual, their family, and community from preschool to adult life. Arch Dis Child 90(Suppl 1):i2–7CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Matza LS, Paramore C, Prasad M (2005) A review of the economic burden of ADHD. Cost Eff Resour Alloc 3:5CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Polanczyk G, de Lima MS, Horta BL, Biederman J, Rohde LA (2007) The worldwide prevalence of ADHD: a systematic review and metaregression analysis. Am J Psychiatry 164:942–948CrossRefPubMedGoogle Scholar
  4. 4.
    Polanczyk G, Rohde LA (2007) Epidemiology of attention-deficit/hyperactivity disorder across the lifespan. Curr Opin Psychiatry 20:386–392CrossRefPubMedGoogle Scholar
  5. 5.
    Faraone SV, Perlis RH, Doyle AE, Smoller JW, Goralnick JJ, Holmgren MA, Sklar P (2005) Molecular genetics of attention-deficit/hyperactivity disorder. Biol Psychiatry 57:1313–1323CrossRefPubMedGoogle Scholar
  6. 6.
    Scahill L, Schwab-Stone M, Merikangas KR, Leckman JF, Zhang H, Kasl S (1999) Psychosocial and clinical correlates of ADHD in a community sample of school-age children. J Am Acad Child Adolesc Psychiatry 38:976–984CrossRefPubMedGoogle Scholar
  7. 7.
    Edwards MC, Schulz EG, Long N (1995) The role of the family in the assessment of attention deficit hyperactivity disorder. Clin Psychol Rev 15:375–394CrossRefGoogle Scholar
  8. 8.
    Banerjee TD, Middleton F, Faraone SV (2007) Environmental risk factors for attention-deficit hyperactivity disorder. Acta Paediatr 96:1269–1274CrossRefPubMedGoogle Scholar
  9. 9.
    Langley K, Holmans PA, van den Bree MB, Thapar A (2007) Effects of low birth weight, maternal smoking in pregnancy and social class on the phenotypic manifestation of attention deficit hyperactivity disorder and associated antisocial behaviour: investigation in a clinical sample. BMC Psychiatry 7:26CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Obel C, Linnet KM, Henriksen TB, Rodriguez A, Jarvelin MR, Kotimaa A, Moilanen I, Ebeling H, Bilenberg N, Taanila A, Ye G, Olsen J (2009) Smoking during pregnancy and hyperactivity-inattention in the offspring—comparing results from three Nordic cohorts. Int J Epidemiol 38:698–705CrossRefPubMedGoogle Scholar
  11. 11.
    Zhu JL, Olsen J, Liew Z, Li J, Niclasen J, Obel C (2014) Parental smoking during pregnancy and ADHD in children: the Danish national birth cohort. Pediatrics 134:e382–388CrossRefPubMedGoogle Scholar
  12. 12.
    Biederman J, Martelon M, Woodworth KY, Spencer TJ, Faraone SV (2014) Is maternal smoking during pregnancy a risk factor for cigarette smoking in offspring? a longitudinal controlled study of ADHD children grown up. J Atten Disord. doi: 10.1177/1087054714557357 Google Scholar
  13. 13.
    Han JY, Kwon HJ, Ha M, Paik KC, Lim MH, Gyu Lee S, Yoo SJ, Kim EJ (2015) The effects of prenatal exposure to alcohol and environmental tobacco smoke on risk for ADHD: a large population-based study. Psychiatry Res 225:164–168CrossRefPubMedGoogle Scholar
  14. 14.
    Sagiv SK, Epstein JN, Bellinger DC, Korrick SA (2013) Pre- and postnatal risk factors for ADHD in a nonclinical pediatric population. J Atten Disord 17:47–57CrossRefPubMedGoogle Scholar
  15. 15.
    Melchior M, Hersi R, van der Waerden J, Larroque B, Saurel-Cubizolles MJ, Chollet A, Galera C (2015) Maternal tobacco smoking in pregnancy and children’s socio-emotional development at age 5: the EDEN mother-child birth cohort study. Eur Psychiatry 30:562–568CrossRefPubMedGoogle Scholar
  16. 16.
    Kovess V, Keyes KM, Hamilton A, Pez O, Bitfoi A, Koc C, Goelitz D, Kuijpers R, Lesinskiene S, Mihova Z, Otten R, Fermanian C, Pilowsky DJ, Susser E (2015) Maternal smoking and offspring inattention and hyperactivity: results from a cross-national European survey. Eur Child Adolesc Psychiatry 24:919–929CrossRefPubMedGoogle Scholar
  17. 17.
    Button TM, Maughan B, McGuffin P (2007) The relationship of maternal smoking to psychological problems in the offspring. Early Hum Dev 83:727–732CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Palmer RH, Bidwell LC, Heath AC, Brick LA, Madden PA, Knopik VS (2016) Effects of maternal smoking during pregnancy on offspring externalizing problems: contextual effects in a sample of female twins. Behav Genet 46:403–415CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Bidwell LC, Palmer RH, Brick L, Madden PA, Heath AC, Knopik VS (2016) A propensity scoring approach to characterizing the effects of maternal smoking during pregnancy on offspring’s initial responses to cigarettes and alcohol. Behav Genet 46:416–430CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Boutwell BB, Beaver KM (2010) Maternal cigarette smoking during pregnancy and offspring externalizing behavioral problems: a propensity score matching analysis. Int J Environ Res Public Health 7:146–163CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    D’Onofrio BM, Class QA, Rickert ME, Larsson H, Langstrom N, Lichtenstein P (2013) Preterm birth and mortality and morbidity: a population-based quasi-experimental study. JAMA Psychiatry 70:1231–1240CrossRefPubMedGoogle Scholar
  22. 22.
    Pettersson E, Sjolander A, Almqvist C, Anckarsater H, D’Onofrio BM, Lichtenstein P, Larsson H (2015) Birth weight as an independent predictor of ADHD symptoms: a within-twin pair analysis. J Child Psychol Psychiatry 56:453–459CrossRefPubMedGoogle Scholar
  23. 23.
    Hultman CM, Torrang A, Tuvblad C, Cnattingius S, Larsson JO, Lichtenstein P (2007) Birth weight and attention-deficit/hyperactivity symptoms in childhood and early adolescence: a prospective Swedish twin study. J Am Acad Child Adolesc Psychiatry 46:370–377CrossRefPubMedGoogle Scholar
  24. 24.
    Mann JR, McDermott S (2011) Are maternal genitourinary infection and pre-eclampsia associated with ADHD in school-aged children? J Atten Disord 15:667–673CrossRefPubMedGoogle Scholar
  25. 25.
    Thapar A, Cooper M, Eyre O, Langley K (2013) What have we learnt about the causes of ADHD? J Child Psychol Psychiatry 54:3–16CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Pasker-de Jong PC, Zielhuis GA, van Gelder MM, Pellegrino A, Gabreels FJ, Eskes TK (2010) Antihypertensive treatment during pregnancy and functional development at primary school age in a historical cohort study. BJOG 117:1080–1086CrossRefPubMedGoogle Scholar
  27. 27.
    Pringsheim T, Sandor P, Lang A, Shah P, O’Connor P (2009) Prenatal and perinatal morbidity in children with Tourette syndrome and attention-deficit hyperactivity disorder. J Dev Behav Pediatr 30:115–121CrossRefPubMedGoogle Scholar
  28. 28.
    Rand KM, Austin NC, Inder TE, Bora S, Woodward LJ (2016) Neonatal infection and later neurodevelopmental risk in the very preterm infant. J Pediatr 170:97–104CrossRefPubMedGoogle Scholar
  29. 29.
    Ahrens W, Bammann K, Siani A, Buchecker K, De Henauw S, Iacoviello L, Hebestreit A, Krogh V, Lissner L, Marild S, Molnar D, Moreno LA, Pitsiladis YP, Reisch L, Tornaritis M, Veidebaum T, Pigeot I, Consortium I (2011) The IDEFICS cohort: design, characteristics and participation in the baseline survey. Int J Obesity 35(Suppl 1):S3–15CrossRefGoogle Scholar
  30. 30.
    Russell G, Ford T, Rosenberg R, Kelly S (2014) The association of attention deficit hyperactivity disorder with socioeconomic disadvantage: alternative explanations and evidence. J Child Psychol Psychiatry 55:436–445CrossRefPubMedGoogle Scholar
  31. 31.
    UNESCO (2012) International standard classification of education ISCED 2011. In: UNESCO Institute for Statistics Montreal, CanadaGoogle Scholar
  32. 32.
    Cole TJ, Lobstein T (2012) Extended international (IOTF) body mass index cut-offs for thinness, overweight and obesity. Pediatr Obes 7:284–294. doi: 10.1111/j.2047-6310.2012.00064.x CrossRefPubMedGoogle Scholar
  33. 33.
    Skogli EW, Teicher MH, Andersen PN, Hovik KT, Oie M (2013) ADHD in girls and boys—gender differences in co-existing symptoms and executive function measures. BMC Psychiatry 13:298CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Barkley RA (2006) Attention-deficit hyperactivity disorder: a handbook for diagnosis and treatment. The Guilford Press, New York CityGoogle Scholar
  35. 35.
    Polanczyk GV, Salum GA, Sugaya LS, Caye A, Rohde LA (2015) Annual research review: a meta-analysis of the worldwide prevalence of mental disorders in children and adolescents. J Child Psychol Psychiatry 56:345–365CrossRefPubMedGoogle Scholar
  36. 36.
    Rucklidge JJ (2010) Gender differences in attention-deficit/hyperactivity disorder. Psychiatr Clin N Am 33:357–373CrossRefGoogle Scholar
  37. 37.
    Langley K, Rice F, van den Bree MB, Thapar A (2005) Maternal smoking during pregnancy as an environmental risk factor for attention deficit hyperactivity disorder behaviour. A review. Minerva Pediatr 57:359–371PubMedGoogle Scholar
  38. 38.
    Linnet KM, Dalsgaard S, Obel C, Wisborg K, Henriksen TB, Rodriguez A, Kotimaa A, Moilanen I, Thomsen PH, Olsen J, Jarvelin MR (2003) Maternal lifestyle factors in pregnancy risk of attention deficit hyperactivity disorder and associated behaviors: review of the current evidence. Am J Psychiatry 160:1028–1040CrossRefPubMedGoogle Scholar
  39. 39.
    Roza SJ, Verhulst FC, Jaddoe VW, Steegers EA, Mackenbach JP, Hofman A, Tiemeier H (2009) Maternal smoking during pregnancy and child behaviour problems: the Generation R Study. Int J Epidemiol 38:680–689CrossRefPubMedGoogle Scholar
  40. 40.
    Knopik VS (2009) Maternal smoking during pregnancy and child outcomes: real or spurious effect? Dev Neuropsychol 34:1–36CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Obel C, Zhu JL, Olsen J, Breining S, Li J, Gronborg TK, Gissler M, Rutter M (2016) The risk of attention deficit hyperactivity disorder in children exposed to maternal smoking during pregnancy—a re-examination using a sibling design. J Child Psychol Psychiatry 57:532–537CrossRefPubMedGoogle Scholar
  42. 42.
    Thapar A, Rice F, Hay D, Boivin J, Langley K, van den Bree M, Rutter M, Harold G (2009) Prenatal smoking might not cause attention-deficit/hyperactivity disorder: evidence from a novel design. Biol Psychiatry 66:722–727CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Chudal R, Joelsson P, Gyllenberg D, Lehti V, Leivonen S, Hinkka-Yli-Salomaki S, Gissler M, Sourander A (2015) Parental age and the risk of attention-deficit/hyperactivity disorder: a nationwide, population-based cohort study. J Am Acad Child Adolesc Psychiatry 54(487–494):e481Google Scholar
  44. 44.
    Silva D, Colvin L, Hagemann E, Bower C (2014) Environmental risk factors by gender associated with attention-deficit/hyperactivity disorder. Pediatrics 133:e14–22CrossRefPubMedGoogle Scholar
  45. 45.
    Chang Z, Lichtenstein P, D’Onofrio BM, Almqvist C, Kuja-Halkola R, Sjolander A, Larsson H (2014) Maternal age at childbirth and risk for ADHD in offspring: a population-based cohort study. Int J Epidemiol 43:1815–1824CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Mersky JP, Reynolds AJ (2007) Child maltreatment and violent delinquency: disentangling main effects and subgroup effects. Child Maltreat 12:246–258CrossRefPubMedGoogle Scholar
  47. 47.
    Xie H, Cairns BD, Cairns RB (2001) Predicting teen motherhood and teen fatherhood: individual characteristics and peer affiliations. Soc Dev 10:488–511CrossRefGoogle Scholar
  48. 48.
    Russell AE, Ford T, Russell G (2015) Socioeconomic associations with ADHD: findings from a mediation analysis. PLoS ONE 10:e0128248CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Coyne CA, Långström N, Rickert ME, Lichtenstein P, D’Onofrio BM (2013) Maternal age at first birth and offspring criminality: using the children-of-twins design to test causal hypotheses. Dev Psychopathol 25:17–35CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Allen VM, Joseph K, Murphy KE, Magee LA, Ohlsson A (2004) The effect of hypertensive disorders in pregnancy on small for gestational age and stillbirth: a population based study. BMC Pregnancy Childbirth 4:17CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Groom KM, North RA, Poppe KK, Sadler L, McCowan LM (2007) The association between customised small for gestational age infants and pre-eclampsia or gestational hypertension varies with gestation at delivery. BJOG 114:478–484CrossRefPubMedGoogle Scholar
  52. 52.
    Silva D, Colvin L, Hagemann E, Stanley F, Bower C (2014) Children diagnosed with attention deficit disorder and their hospitalisations: population data linkage study. Eur Child Adolesc Psychiatry 23:1043–1050CrossRefPubMedGoogle Scholar
  53. 53.
    Silk TJ, Vance A, Rinehart N, Bradshaw JL, Cunnington R (2009) White-matter abnormalities in attention deficit hyperactivity disorder: a diffusion tensor imaging study. Hum Brain Mapp 30:2757–2765CrossRefPubMedGoogle Scholar
  54. 54.
    Inder TE, Wells SJ, Mogridge NB, Spencer C, Volpe JJ (2003) Defining the nature of the cerebral abnormalities in the premature infant: a qualitative magnetic resonance imaging study. J Pediatr 143:171–179CrossRefPubMedGoogle Scholar
  55. 55.
    Chau V, Brant R, Poskitt KJ, Tam EW, Synnes A, Miller SP (2012) Postnatal infection is associated with widespread abnormalities of brain development in premature newborns. Pediatr Res 71:274–279CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Reich W, Todd RD, Joyner CA, Neuman RJ, Heath AC (2003) Reliability and stability of mothers’ reports about their pregnancies with twins. Twin Res 6:85–88CrossRefPubMedGoogle Scholar
  57. 57.
    Tomeo CA, Rich-Edwards JW, Michels KB, Berkey CS, Hunter DJ, Frazier AL, Willett WC, Buka SL (1999) Reproducibility and validity of maternal recall of pregnancy-related events. Epidemiology 10:774–777CrossRefPubMedGoogle Scholar
  58. 58.
    Heath AC, Knopik VS, Madden PA, Neuman RJ, Lynskey MJ, Slutske WS, Jacob T, Martin NG (2003) Accuracy of mothers’ retrospective reports of smoking during pregnancy: comparison with twin sister informant ratings. Twin Res 6:297–301CrossRefPubMedGoogle Scholar
  59. 59.
    Patrick DL, Cheadle A, Thompson DC, Diehr P, Koepsell T, Kinne S (1994) The validity of self-reported smoking: a review and meta-analysis. Am J Public Health 84:1086–1093CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Hermann Pohlabeln
    • 1
    Email author
  • Stefan Rach
    • 1
  • Stefaan De Henauw
    • 2
  • Gabriele Eiben
    • 3
  • Wencke Gwozdz
    • 4
  • Charalampos Hadjigeorgiou
    • 5
  • Dénes Molnár
    • 6
  • Luis A. Moreno
    • 7
  • Paola Russo
    • 8
  • Toomas Veidebaum
    • 9
  • Iris Pigeot
    • 1
  • On behalf of the IDEFICS consortium
  1. 1.Leibniz Institute for Prevention Research and Epidemiology—BIPSBremenGermany
  2. 2.Department of Public Health, Faculty of Medicine and Health SciencesGhent UniversityGhentBelgium
  3. 3.Section for Epidemiology and Social Medicine, Institute of MedicineSahlgrenska Academy, University of GothenburgGothenburgSweden
  4. 4.Department of Intercultural Communication and Management, Centre for Corporate Social ResponsibilityCopenhagen Business SchoolCopenhagenDenmark
  5. 5.Research and Education Institute of Child HealthStrovolosCyprus
  6. 6.Department of Paediatrics, Medical FacultyUniversity of PécsPecsHungary
  7. 7.GENUD (Growth, Exercise, Nutrition and Development) Research Group, Instituto Agroalimentario de Aragón (IA2), Instituto de Investigación Sanitaria Aragón (IIS Aragón), Centro de Investigación Biomédica en Red Fisiopatología de la Obesidad y Nutrición (CIBERObn)University of ZaragozaSaragossaSpain
  8. 8.Unit of Epidemiology & Population Genetics, Institute of Food SciencesNational Research CouncilAvellinoItaly
  9. 9.National Institute for Health DevelopmentTallinnEstonia

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